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Organized Ribosome-Containing Structural Domains in Axons

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Cell Biology of the Axon

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 48))

Abstract

Periaxoplasmic ribosomal plaques (PARPs) are systematically recurring ribosome-containing structural domains located in the F-actin-rich periphery of axoplasm in myelinated fibers. In contrast, endoaxoplasmic ribosomal plaques (EARPs) are small, oval-shaped ribosomal aggregate structures randomly dispersed within the axoplasm of unmyelinated squid giant axons. Ribosomes are attached to a superficial plaque-like structural matrix, which “caps” the domain at the outer cortical margin and appears fragmented in subcortical axoplasm. As such, the matrix represents a novel hallmark of PARP domains. Molecular markers concentrated in PARP domains include β-actin mRNA, ZBP-1, SRP54, myosin Va and kinesin II molecular motor proteins. Rapid axoplasmic transport of microinjected heterologous radiolabeled BC1 RNA to putative PARP domains, mediated pari passu by microtubule- and F-actin-dependent systems, suggests that translation machinery, anchored by the matrix could provide targeted destinations for RNA trafficking. As distributed local centers of protein synthesis along axons, PARPs are likely to share modes of expression in common with other translational subdomains in neurons.

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References

  • Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS (1998) Sorting of β-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 18:251–265

    PubMed  CAS  Google Scholar 

  • Bazzet-Jones DP (1988) Phosphorus imaging of the 7-S ribonucleoprotein particle. J Ultrastr Mol Struct Res 99:59–69

    Article  Google Scholar 

  • Bleher R , Martin R (2001) Ribosomes in the squid giant axon. Neuroscience 107:527–534

    Article  PubMed  CAS  Google Scholar 

  • Bramham CR, Wells DG (2007) Dendritic mRNA: transport, translation and function. Nature Rev Neurosci 8:776–787

    Article  CAS  Google Scholar 

  • Brittis PA, Lu Q, Flanagan JG (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110:223–235

    Article  PubMed  CAS  Google Scholar 

  • Conradi S (1966) Ultrastructural specialization in the initial segment of cat lumber motoneurons. Acta Soc Med Upsalien 71:281–284

    CAS  Google Scholar 

  • Court FA, Hendriks WTJ, MacGillavry HD, Alvarez J, van Minnen J (2008) Novel understanding of the role of glia in the nervous system. J Neurosci 28:11024–1102

    Article  PubMed  CAS  Google Scholar 

  • Crispino M, Castigli E, Perrone Capano C, Martin R, Menichini E, Kaplan BB, Giuditta A (1993) Protein synthesis in a synaptosomal fraction from squid brain. Mol Cell Neurosci 4:366–374

    Article  PubMed  CAS  Google Scholar 

  • Crispino M, Kaplan BB, Martin R , Alvarez J, Chun JT, Benech JC, Giuditta A (1997) Active polysomes are present in the large presynaptic endings of the synaptosomal fraction from squid brain. J Neurosci 17:7694–7702

    PubMed  CAS  Google Scholar 

  • Door R, Richter K, Martin R (1997) Detection of low phosphorus contents in neurofilaments of squid axons by image-EELS contrast spectroscopy. J Microsc 188:173–181

    Article  PubMed  CAS  Google Scholar 

  • Edström A (1964a) The ribonucleic acid in the Mauthner neuron of the goldfish. J Neurochem 11:309–314

    Article  Google Scholar 

  • Edström A (1964b) Effect of spinal cord transection on the base composition and content of RNA in the Mauthner nerve fibre of the goldfish. J Neurochem 11:557–559

    Article  Google Scholar 

  • Edström A, Sjöstrand J (1969) Protein synthesis in isolated Mauthner nerve fibre components. J Neurochem 16:67–81

    Article  PubMed  Google Scholar 

  • Edström J-E, Eichner D, Edström A (1962) The ribonucleic acid of axons and myelin sheaths from Mauthner neurons. Biochim Biophys Acta 61:178–184

    PubMed  Google Scholar 

  • Gioio AE, Chun JT, Crispino M, Perrone Capano C, Giuditta A, Kaplan BB (1994) Kinesin mRNA is present in the squid giant axon. J Neurochem 63:3–18

    Google Scholar 

  • Giuditta A, Metafora S, Felsani A, Del Rio A (1977) Factors for protein synthesis in the axoplasm of squid giant axons. J Neurochem 28:1393–1395

    Article  PubMed  CAS  Google Scholar 

  • Giuditta A, Cupello A, Lazzarini G (1980) Ribosomal RNA in the axoplasm of the squid giant axon. J Neurochem 34:1757–1760

    Article  PubMed  CAS  Google Scholar 

  • Giuditta A, Menichini E, Perrone Capano C, Langella M, Martin R, Castigli E, Kaplan BB (1991) Active polysomes in the axoplasm of the squid giant axon. J Neurosci Res 26:18–28

    Article  Google Scholar 

  • Giuditta A, Chun JT, Eyman M, Cefaliello C, Bruno PA, Crispino M (2008) Local gene expression in axons and nerve endings: the glia-neuron unit. Physiol Rev 88:515–555

    Article  PubMed  CAS  Google Scholar 

  • Hillefors M, Gioio AE, Mameza MG, Kaplan BB (2007) Axon viability and mitochondrial function are dependent on local protein synthesis in sympathetic neurons. Cell Mol Neurobiol 27:701–716

    Article  PubMed  CAS  Google Scholar 

  • Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. 70:755–777

    Google Scholar 

  • Kindler S, Wang H, Richter D, Tiedge H (2005) RNA transport and local control of translation. Annu Rev Cell Dev Biol 21:223–245

    Article  PubMed  CAS  Google Scholar 

  • Koenig E (1965) Synthetic mechanisms in the axon. Part II: RNA in myelin-free axons of the cat. J Neurochem 12:357–361

    Article  PubMed  CAS  Google Scholar 

  • Koenig E (1979) Ribosomal RNA in Mauthner axon: implications for a protein synthesizing machinery in the myelinated axon. Brain Res 174:95–107

    Article  PubMed  CAS  Google Scholar 

  • Koenig E (1991) Evaluation of local synthesis of axonal proteins in goldfish Mauthner cell axon and axons of dorsal and ventral roots of the rat in vitro. Mol Cell Neurosci 2:384–394

    Article  PubMed  CAS  Google Scholar 

  • Koenig E, Adams P (1982) Local protein synthesizing activity in axonal fields regenerating in vitro. J Neurochem 39:386–400

    Article  PubMed  CAS  Google Scholar 

  • Koenig E, Martin R (1996) Cortical plaque-like structures identify ribosome- containing domains in the Mauthner axon. J Neurosci 16:1400–1411

    PubMed  CAS  Google Scholar 

  • Koenig E, Martin R, Titmus M, Sotelo-Silveira JR (2000) Cryptic peripheral ribosomal domains distributed intermittently along mammalian myelinated axons. J Neurosci 20:8390–8400

    PubMed  CAS  Google Scholar 

  • Korn AP, Spitnik-Elson P, Elson D (1983) Specific visualization of ribosomal RNA in intact ribosomes by electron spectroscopic imaging. Eur J Cell Biol 31:334–340

    PubMed  CAS  Google Scholar 

  • Kun A, Otero L, Sotelo-Silveira JR, Sotelo JR (2007) Ribosomal distributions in axons of mammalian myelinated fibers. J Neurosci Res 85:2087–2098

    Article  PubMed  CAS  Google Scholar 

  • Lee S-K, Hollenbeck PJ (2003) Organization and translation of mRNA in sympathetic axons. J Cell Sci 116:4467–4478

    Article  PubMed  CAS  Google Scholar 

  • Lerner EA, Lerner MR, Janeway CA Jr, Steitz JA (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci U S A 78:2737–2741

    Article  PubMed  CAS  Google Scholar 

  • Martin R, Fritz W, Giuditta A (1989) Visualization of polyribosomes in the postsynaptic area of the squid giant synapse by electron spectroscopic imaging. J Neurocytol 18:11–18

    Article  PubMed  CAS  Google Scholar 

  • Martin R, Vaida B, Bleher R, Crispino M, Giuditta A (1998) Protein synthesizing units in presynaptic and postsynaptic domains of squid neurons. J Cell Sci 111:3157–3166

    PubMed  CAS  Google Scholar 

  • Merianda TT, Lin A, Lam J, Vuppalanchi D, Willis, DE, Karin N, Holt CE, Twiss JL (2008) A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol Cell Neurosc doi:10.1016/j.mcn.2008.09.008

    Google Scholar 

  • Muslimov IA, Santi E, Homel P, Perini S, Higgins D and Tedge H (1997) RNA transport in dendrites: cis-acting targeting element is contained within neuronal BC1 RNA. J Neurosci 17:4722–4733

    PubMed  CAS  Google Scholar 

  • Muslimov IA, Titmus M, Koenig E, Tiedge H (2002) Transport of neuronal BC1 RNA in Mauthner axons. J Neurosci 22:4293–4301

    PubMed  CAS  Google Scholar 

  • Ottensmeyer FP (1986) Elemental mapping by energy filtration: advantages, limitations and compromises. Ann NY Acad Sci 483:339–353.

    Article  PubMed  CAS  Google Scholar 

  • Palay SL, Sotelo C, Peters A, Orkland PM (1968) The axon hillock and the initial segment. J Cell Biol 38:193–201

    Article  PubMed  CAS  Google Scholar 

  • Pannese E, Ledda M (1991) Ribosomes in myelinated axons of the rabbit spinal ganglion neurons. J Submicrosc Cytol Pathol 23:33–38

    PubMed  CAS  Google Scholar 

  • Peters A, Proskauer CG, Kaiserman-Abramof IR (1968) The small pyramidal neuron of the cat cerebral cortex. The axon hillock and the initial segment. J Cell Biol 39: 604–619

    Article  PubMed  CAS  Google Scholar 

  • Sato M, Wong TZ, Brown DT, Allen RD (1984) Rheological properties of living cytoplasm: a preliminary investigation of squid axoplasm (Loligo pealei). Cell Motil 4:7–23

    Article  PubMed  CAS  Google Scholar 

  • Sotelo JR, Kun A, Benech JC, Giuditta A, Morillas J, Benech CR (1999) Ribosomes and polyribosomes are present in the squid giant axon: an immunocytochemical study. Neuroscience 90:705–715

    Article  PubMed  CAS  Google Scholar 

  • Sotelo-Silveira JR, Calliari A, Cárdenas M, Koenig E, Sotelo JR (2004) Myosin Va and kinesin II motor proteins are concentrated in ribosomal domains (periaxoplasmic ribosomal plaques) of myelinated axons. J Neurobiol 60:187–196

    Article  PubMed  CAS  Google Scholar 

  • Sotelo-Silveira J, Crispino M, Puppo A, Sotelo JR, Koenig E (2008) Myelinated axons contain b-actin mRNA and ZBP-1 in periaxoplasmic ribosomal plaques and depend on cyclic AMP and F-actin integrity for in vitro translation. J Neurochem 104:545–557

    PubMed  CAS  Google Scholar 

  • Spencer GE, Syed NI, van Kesteren E, Lukowiak K, Geraerts WP, van Minnen J (2000) Synthesis and functional integration of a neurotransmitter receptor in isolated invertebrate axons. J Neurobiol 44:72–81

    Article  PubMed  CAS  Google Scholar 

  • Walter P, Blobel G (1983) Subcellular distribution signal recognition particle and 7SL-RNA determined with polypeptide-specific antibodies and complementary DNA probe. J Cell Biol 97:1693–1699

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Iacoangeli A, Popp A, Muslimov IA, Imataka H, Sonenberg N, Lomakin IB, Tiedge H (2002) Dendritic BC1 RNA: functional role in regulation of translation initiation. J Neurosci 22:10232–10241

    PubMed  CAS  Google Scholar 

  • Zelenà J (1972) Ribosomes in myelinated axons of dorsal root ganglia. Z Zellforsch 124:217–229

    Article  PubMed  Google Scholar 

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  1. Department of Physiology and Biophysics, SUNY at Buffalo School of Medicine, Buffalo, NY, 14214-3013, USA

    Edward Koenig

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    Edward Koenig

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Koenig, E. (2009). Organized Ribosome-Containing Structural Domains in Axons. In: Koenig, E. (eds) Cell Biology of the Axon. Results and Problems in Cell Differentiation, vol 48. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2008_29

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